Evidence for a Large-Scale Brain System Supporting Allostasis and Interoception in Humans

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Abstract

Large-scale intrinsic brain systems have been identified for exteroceptive senses (e.g., sight, hearing, touch). We introduce an analogous system for representing sensations from within the body, called interoception, and demonstrate its relation to regulating peripheral systems in the body, called allostasis. Employing the recently introduced Embodied Predictive Interoception Coding (EPIC) model, we used tract-tracing studies of macaque monkeys, followed by two intrinsic functional magnetic resonance imaging samples ( N = 280 and N = 270) to evaluate the existence of an intrinsic allostatic/interoceptive system in the human brain. Another sample ( N = 41) allowed us to evaluate the convergent validity of the hypothesized allostatic/interoceptive system by showing that individuals with stronger connectivity between system hubs performed better on an implicit index of interoceptive ability related to autonomic fluctuations. Implications include insights for the brain’s functional architecture, dissolving the artificial boundary between mind and body, and unifying mental and physical illness.

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The organization of the human cerebral cortex estimated by intrinsic functional connectivity.

B T Thomas Yeo, Fenna M Krienen, Jorge Sepulcre … (2011)

Information processing in the cerebral cortex involves interactions among distributed areas. Anatomical connectivity suggests that certain areas form local hierarchical relations such as within the visual system. Other connectivity patterns, particularly among association areas, suggest the presence of large-scale circuits without clear hierarchical relations. In this study the organization of networks in the human cerebrum was explored using resting-state functional connectivity MRI. Data from 1,000 subjects were registered using surface-based alignment. A clustering approach was employed to identify and replicate networks of functionally coupled regions across the cerebral cortex. The results revealed local networks confined to sensory and motor cortices as well as distributed networks of association regions. Within the sensory and motor cortices, functional connectivity followed topographic representations across adjacent areas. In association cortex, the connectivity patterns often showed abrupt transitions between network boundaries. Focused analyses were performed to better understand properties of network connectivity. A canonical sensory-motor pathway involving primary visual area, putative middle temporal area complex (MT+), lateral intraparietal area, and frontal eye field was analyzed to explore how interactions might arise within and between networks. Results showed that adjacent regions of the MT+ complex demonstrate differential connectivity consistent with a hierarchical pathway that spans networks. The functional connectivity of parietal and prefrontal association cortices was next explored. Distinct connectivity profiles of neighboring regions suggest they participate in distributed networks that, while showing evidence for interactions, are embedded within largely parallel, interdigitated circuits. We conclude by discussing the organization of these large-scale cerebral networks in relation to monkey anatomy and their potential evolutionary expansion in humans to support cognition.

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Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion.

Jonathan D Power, Kelly A Barnes, Abraham Z Snyder … (2012)

Here, we demonstrate that subject motion produces substantial changes in the timecourses of resting state functional connectivity MRI (rs-fcMRI) data despite compensatory spatial registration and regression of motion estimates from the data. These changes cause systematic but spurious correlation structures throughout the brain. Specifically, many long-distance correlations are decreased by subject motion, whereas many short-distance correlations are increased. These changes in rs-fcMRI correlations do not arise from, nor are they adequately countered by, some common functional connectivity processing steps. Two indices of data quality are proposed, and a simple method to reduce motion-related effects in rs-fcMRI analyses is demonstrated that should be flexibly implementable across a variety of software platforms. We demonstrate how application of this technique impacts our own data, modifying previous conclusions about brain development. These results suggest the need for greater care in dealing with subject motion, and the need to critically revisit previous rs-fcMRI work that may not have adequately controlled for effects of transient subject movements. Copyright © 2011 Elsevier Inc. All rights reserved.

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Control of goal-directed and stimulus-driven attention in the brain.

Maurizio Corbetta, Gordon L Shulman (2002)

We review evidence for partially segregated networks of brain areas that carry out different attentional functions. One system, which includes parts of the intraparietal cortex and superior frontal cortex, is involved in preparing and applying goal-directed (top-down) selection for stimuli and responses. This system is also modulated by the detection of stimuli. The other system, which includes the temporoparietal cortex and inferior frontal cortex, and is largely lateralized to the right hemisphere, is not involved in top-down selection. Instead, this system is specialized for the detection of behaviourally relevant stimuli, particularly when they are salient or unexpected. This ventral frontoparietal network works as a 'circuit breaker' for the dorsal system, directing attention to salient events. Both attentional systems interact during normal vision, and both are disrupted in unilateral spatial neglect.

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Author and article information

Journal

Journal ID (nlm-journal-id): 101697750

Journal ID (pubmed-jr-id): 46015

Journal ID (nlm-ta): Nat Hum Behav

Journal ID (iso-abbrev): Nat Hum Behav

Title: Nature human behaviour

ISSN (Electronic): 2397-3374

Publication date Nihms-submitted: 24 February 2017

Publication date (Electronic): 24 April 2017

Publication date (Print): 2017

Publication date PMC-release: 24 October 2017

Volume: 1

Electronic Location Identifier: 0069

Affiliations

[1 ]Department of Psychology, Northeastern University, Boston, MA

[2 ]Department of Neurology, Massachusetts General Hospital and Harvard Medical School

[3 ]Athinoula A. Martinos Center for Biomedical Imaging

[4 ]Psychiatric Neuroimaging Division, Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA

[5 ]Frontotemporal Disorders Unit, Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA

[6 ]Laureate Institute for Brain Research, Tulsa, OK

[7 ]School of Community Medicine, The University of Tulsa, Tulsa, OK

[8 ]Edith Nourse Rogers Memorial VA Hospital, Bedford, MA

Author notes

[* ]Corresponding authors: ian_kleckner@ 123456urmc.rochester.edu , l.barrett@ 123456neu.edu

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Manuscript ID: NIHMS852367

DOI: 10.1038/s41562-017-0069

PMC ID: 5624222

PubMed ID: 28983518

SO-VID: 808938b4-b055-4456-9b2c-733eba372a42

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Evidence for a Large-Scale Brain System Supporting Allostasis and Interoception in Humans

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Abstract

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Most cited references 255

The organization of the human cerebral cortex estimated by intrinsic functional connectivity.

Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion.

Control of goal-directed and stimulus-driven attention in the brain.

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